Climatic variation and seed persistence: freeze–thaw cycles lower survival via the joint action of abiotic stress and fungal pathogens

Abstract

Global climate change is altering thermal cycles in soils during late winter, a transition that may directly threaten seed survival via abiotic stress, facilitate infection by soil-borne pathogens, or both. Using field-collected soil and seeds of the perennial bunchgrass Elymus canadensis, we tested the hypothesis that soil freeze-thaw events limit survival within the soil through direct effects on seed persistence and amplification of soil pathogen attack using a factorial experiment that manipulated freeze-thaw cycles (constant freeze vs. freeze-thaw) and fungicide addition. Freeze-thaw treatment resulted in lower seedling emergence and delayed emergence time relative to constant-freeze controls. Fungicide-treated soils had greater emergence relative to untreated soils; the lowest seedling emergence was observed in no-fungicide, freeze-thaw-treated soils (<1 %). The strong effects of thermal variability and fungi on seeds were mitigated through interactions at the seed-soil interface, as subsequent experiments showed that fungicide and freeze-thaw treatments alone do not influence dormancy. Our work demonstrates that changes in freeze-thaw events directly limit seedling emergence, delay seedling phenology, and provide opportunities for fungal pathogens to limit seed persistence. As recruitment from seeds is a key determinant of plant population dynamics, these results suggest that climatic variation may generate unique consequences for populations under changing climate regimes.

Exogenous application of methyl jasmonate altersPinus resinosaseedling response to simulated frost

“…Variation in temperature regimes are an inextricable component of climate change and can represent a significant barrier to plant survival and growth (Kreyling 2010;Hufkens et al 2012;Connolly and Orrock 2015). Our ability to understand how shifts in temperature regime will influence plant populations relies on understanding how multiple different stresses interact to shape an individual plant's survival and growth.…”

Past freeze–thaw events on Pinus seeds increase seedling herbivory

“…). Cold stress can shape the demography of temperate terrestrial vegetation (Kreyling ), with recent studies highlighting how untimely cold stress can strongly affect seed viability (Connolly and Orrock ), juvenile survival (Augspurger ), and adult performance and reproduction (Gu et al. , Inouye ).…”

“…Field soil was collected from a central Wisconsin forest (Dexter County Park, Wood Co.; latitude 44.39°; longitude −90.13°) dominated by Acer saccahrum, Acer rubrum , and Quercus rubra with associated P. resinosa and P. strobus . We collected soil during late February to ensure that soil physical composition and microbial communities reflect the status of the region's soils prior to the onset of natural freeze–thaw cycles (Henry , Connolly and Orrock ). Snow was removed and mineral soil was exhumed to a depth of 5 cm from three 1 × 1 m plots located along a straight east–west transect; the center of each plot was 10 m apart.…”

“…Aliquots of 35 mL of soil were put into separate, sterile 50‐mL centrifuge tubes. When soil was partitioned into centrifuge tubes, soil was handled in small batches (~200–300 mL) in multiple sessions to minimize the amount of time soil was handled outside refrigeration (Connolly and Orrock ). Eight cold‐stratified P. strobus or P. resinosa seeds were added to each tube, which was capped and slowly inverted twice to distribute the seeds within the mineral soil.…”

“…In temperate and boreal ecosystems, juvenile plants and plant propagules overwintering at the soil–atmosphere interface may be injured or killed if exposed to soil freezing (de Chantal et al. , Connolly and Orrock ). Although evidence suggests that, in mature plants, negative effects of cold stress can manifest up to a year after extreme cold events (Kreyling , Lacoste et al.…”